Accepted Article

Received Date : 06-May-2014 Accepted Date : 24-Sep-2014 Article type

: Primary Research Articles

Changing gull diet in a changing world: A 150-year stable isotope (δ13C, δ15N) record from

feathers collected in the Pacific Northwest of North America

Running head: Changing gull diet in a changing world

Louise K. Blight1,2,*, Keith A. Hobson3, T. Kurt Kyser4, & Peter Arcese1

1

Centre for Applied Conservation Research, University of British Columbia, 2424 Main Mall,

Vancouver, BC, Canada V6T 1Z4; 2Procellaria Research & Consulting, 944 Dunsmuir Road, Victoria, BC, Canada V9A 5C3; 3Environment Canada, 11 Innovation Blvd., Saskatoon, Canada S7N 3H5; 4Department of Geological Sciences and Geological Engineering, Queen’s University, Kingston, Ontario, Canada K7L 3N6

*

Corresponding author: [email protected]; (+1) 778-677-8495

Keywords: glaucous-winged gull; Larus glaucescens; stable isotope; carbon-13; nitrogen-15; seabird; Salish Sea; shifting baselines; indicator species; environmental change

This article has been accepted for publication and undergone full peer review but has not been through the copyediting, typesetting, pagination and proofreading process, which may lead to differences between this version and the Version of Record. Please cite this article as doi: 10.1111/gcb.12796 This article is protected by copyright. All rights reserved.

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Abstract: The world’s oceans have undergone significant ecological changes following European colonial expansion and associated industrialisation. Seabirds are useful indicators of marine food web structure and can be used to track multi-decadal environmental change, potentially reflecting long-term human impacts. We used stable isotope (δ13C, δ15N) analysis of feathers from

glaucous-winged gulls (Larus glaucescens) in a heavily disturbed region of the northeast Pacific to ask whether diets of this generalist forager changed in response to shifts in food availability over 150 years, and whether any detected change might explain long-term trends in gull abundance. Sampled feathers came from birds collected between 1860 and 2009 at nesting colonies in the Salish Sea, a transboundary marine system adjacent to Washington, USA and British Columbia, Canada. To determine whether temporal trends in stable isotope ratios might simply reflect changes to baseline environmental values, we also analysed muscle tissue from forage fishes collected in the same region over a multi-decadal timeframe. Values of δ13C and δ15N declined since

1860 in both sub-adult and adult gulls (δ13C, ~ 2–6‰; δ15N, ~4–5‰), indicating that their diet has become less marine over time, and that birds now feed at a lower trophic level than previously. Conversely, forage fish δ13C and δ15N values showed no trends, supporting our conclusion that gull feather values were indicative of declines in marine food availability rather than of baseline environmental change. Gradual declines in feather isotope values are consistent with trends predicted had gulls consumed less fish over time, but were equivocal with respect to whether gulls had switched to a more garbage-based diet, or one comprising marine invertebrates. Nonetheless, our results suggest a long-term decrease in diet quality linked to declining fish abundance or other anthropogenic influences, and may help to explain regional population declines in this species and other piscivores.

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Introduction Marine ecosystems worldwide are responding to human-related stressors such as commercial fisheries, climate change, and pollution (Halpern et al., 2008). Effects include degradation or loss of habitat, alteration of food webs, and declines in species richness and abundance, particularly in coastal areas (Roberts & Hawkins 1999; Crain et al., 2009). The profound and potentially ir-

reversible ecological consequences of such changes (Estes et al., 2011) make it important to im-

prove our understanding of them, particularly given their widespread nature and the growing

public concern over ocean health (Crain et al., 2009).

The inshore waters of southern British Columbia and northern Washington, collectively called the Salish Sea, have been ranked among the most disturbed coastal marine ecosystems on Earth (mean cumulative impact score for this region = 19.3, maximum study score = 19.5; Halpern et al., 2008), and as such are targets for more effective conservation and management (Fraser et al.,

2006; Gaydos et al., 2008). However, because of poor and incomplete monitoring, relatively few long-term population trends exist for individual species in the region (Pauly et al., 1998; Gaydos & Pearson 2011), hampering the identification of ecological baselines and conservation targets. In such cases, resident species for which long-term historical data exist stand as potential ecological indicators, particularly when their population growth, life history or diet can be linked to key ecosystem states or processes. Researchers have long recognised seabirds as useful indicators of marine food web structure and temporal changes (Ashmole & Ashmole 1968; Ainley & Boekelheide 1990; Furness & Greenwood 1993; Furness & Camphuysen 1997; Piatt et al., 2007). Marine birds integrate ecosystem change across various spatio-temporal scales, yet as long-lived organisms they can be slow to show signs of alterations in the sampled environment

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(Montevecchi 1993). Conducting studies spanning multiple decades overcomes this potential limitation, while simultaneously providing longer-term perspectives on ecological change. Stable isotope analysis of museum specimens or archaeological samples is increasingly being used to assess long-term dietary changes for various avian taxa (Thompson et al., 1995; Ainley et al., 2006; Becker & Beissinger 2006). For example, Emslie & Patterson (2007) used stable

isotope analysis of eggshell fragments (δ13C in eggshell carbonate; δ15N in eggshell membrane) from subfossil and modern samples to show that Adélie penguins (Pygoscelis adeliae) experienced an abrupt historical shift in diet from fish to krill in the 1700s, coincident with the industrial harvest and depletion of fur seals (Arctocephalus gazella) and whales. Norris et al., (2007) and Gutowsky et al., (2009) similarly used δ13C and δ15N analysis of feathers to link population declines in British Columbia’s marbled murrelet (Brachramphus marmoratus) to declines in fish prey over more than a century. Once grown, feathers are metabolically inert, so their isotopic values reflect diet during the period of feather generation (Mizutani et al., 1990; Hobson 1999). In situations where consumers have access to marine foods, δ13C values generally indicate the relative proportion of pelagic vs. inshore marine or terrestrial foods in the diet, while δ15N values

generally reflect the trophic level at which a bird was feeding at the time of feather growth.

Holarctic Larus gulls occur close to human settlements worldwide and have been studied in detail in many parts of their range, including the Salish Sea (Howell & Dunn 2007). Because gulls have been shown to respond strongly to variation in food availability and environmental change

(Mills et al., 2008), we identified them as a useful focal species for our study region. The glaucous-winged gull (L. glaucescens) is a common, marine-associated bird that has been studied

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and collected for over 150 years (Anonymous 1908; Drent & Guiguet 1961; Hayward & Verbeek 2008). We were thus able to use archived specimens to test whether gulls could be used to determine long-term food web or dietary change in the Salish Sea (cf. Hobson 2007). As a generalist consumer, glaucous-winged gulls should be buffered against ecological change. However, their populations in the Salish Sea increased rapidly during the mid-twentieth century,

growing at c. 2.9% per annum from 1960 to 1986, before declining steeply to less than 50% of peak estimates (Galusha et al., 1987; Vermeer & Devito 1989; Sullivan et al., 2002; Hayward &

Verbeek 2008; Blight et al. in revision). One hypothesis to explain variation in gull population growth invokes evolving waste management practices that first increased and then reduced gull access to garbage (Vermeer & Devito 1989; Vermeer 1992; Hayward et al., 2010). However, there is conflicting evidence as to whether diets including garbage benefit gulls at the population level. For example, glaucous-winged gulls in British Columbia that fed their chicks marine diets (~90% fish) raised offspring that were heavier, grew faster (e.g., for 2-chick broods, mean asymptotic mass of 1014 vs. 883 g; 36 vs. 29 g d-1), and fledged at a higher rate (84% vs. 68%) than those feeding chicks a diet containing garbage (Ward 1973). In the congeneric Western gull L. occidentalis in California, the most successful breeders also avoided garbage and fed themselves and their young primarily on fish (Pierotti & Annett 1990; Annett & Pierotti 1999). These findings imply, all things being equal, that we might expect declines in reproductive performance and population size if glaucous-winged gulls currently consume more garbage than they did historically. Indeed, Blight (2011) showed that glaucous-winged gulls in the Salish Sea have experienced a long-term decline in egg volume and clutch size, consistent with the hypothesis that dietary declines in high-quality fish and an increase in terrestrial sources of food reduces fecundity in this species. Conversely, for European herring gulls (L. argentatus) Spaans (1971) report-

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ed a positive correlation between amount of garbage in diet and brood size, and Pons (1992) reported a decline in reproductive rate coincident with the closure of a garbage disposal site. Given the conflicting results above, we aimed to examine and quantify long-term trends in glaucous-winged gull diets to help elucidate how population trend, diet and environmental change may be linked in this species. Specifically, we used δ13C and δ15N analyses of adult and

sub-adult glaucous-winged gull feathers collected in the Salish Sea between 1860 and 2009 to ask whether and how gull diets changed during the period of rapid human population increase following European colonization, and the associated industrialisation of coastal marine ecosystems in the region. If gull population trends were primarily driven by the declining availability of forage fish (Wallace 1998; Therriault et al., 2009) and other fish foods (e.g., spawning salmon;

Jewett 1953), we expected to observe an indication that the fraction of fish prey in gull diets declined over time, with feather isotope values showing declines in both δ13C and δ15N values as

birds increasingly switched to feeding on marine invertebrates and/or C3-based garbage. Alternatively, we predicted that if glaucous-winged gull population growth was driven primarily by the availability of garbage, isotopic data should reflect an increase in terrestrially-based foods in gull diets up to the mid-1980s (i.e. decreases in δ13C and δ15N values), but a decline thereafter as management practices to restrict access to garbage were established and improved (Pons 1992; Hayward & Verbeek 2008). We further hypothesised that changes in the availability of garbage – or reduction of marine foods in gull diets – would affect sub-adults and adults differently, as

adults are more proficient foragers in marine habitats (Verbeek 1977; Searcy 1978). Given this, and the fact that landfills are often used preferentially by sub-adults (Weiser & Powell 2011), we predicted that gull feather δ13C and δ15N values would indicate a more marine (i.e. higher δ13C and δ15N values) and/or higher trophic level diets for adults than for sub-adults.

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Interpretation of past diets via isotopic data derived over decades or centuries may be confounded by changes to baseline environmental values and it is now recommended that such retrospec-

tive studies address this limitation (e.g., Bond & Jones 2010). For example, the Suess effect describes the reduction in atmospheric δ13C in CO2 as a result of fossil fuel-derived carbon inputs (Gruber et al., 1999; Sonnerup et al., 1999), and this effect ultimately reaches ocean food webs,

which can also show isotopic shifts due to changes in rates of primary productivity (Hilton et al., 2006). Thus, to test for changes to baseline environmental values, we also used δ13C and δ15N measurements of muscle tissue from forage fish collected and archived from the Salish Sea over six decades of our study period.

Materials and methods Study Area Feather samples for stable isotope analyses came from glaucous-winged gull museum skins or moulted feathers collected between 1860 and 2009 (moulted feathers 2009 only) at nesting colonies in the Salish Sea, i.e., the inshore waters of the Strait of Georgia, BC, Canada, adjacent waters of Puget Sound, WA, USA, and the eastern Strait of Juan de Fuca; approximate range: 47.91° – 50.02° N, 121.95° – 125.24° W. This area includes all present-day colonies larger than

10s of pairs within the region, but excludes the more westerly colonies where diet is likely to have been influenced by the offshore marine conditions of the Pacific Ocean. Banding and telemetry data show that most glaucous-winged gulls breeding in the Salish Sea remain in or near the area year-round and that dispersal from natal to breeding sites is local (Pearse 1963; Butler et al. 1980; Reid 1988; J. Elliott, unpubl. data), and thus these birds primarily represent a single

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oceanographic region. This assumption is relevant for stable isotope analysis, because baseline isotope values often vary among regions (Schell et al. 1989; Graham et al., 2010).

Sample Collection and Stable Isotope Analysis – Feathers To assess long-term changes in breeding-season diet we examined changes in δ13C and δ15N val-

ues for a time series of feathers grown in and around the nesting season, a physiologically demanding period when birds must ingest foods that are energetically and nutritionally conducive to successful reproduction (Robbins 1981; Meijer & Drent 1999; Williams 2005). We analysed 270 feather samples from 216 glaucous-winged gulls collected over the 150 y study period. Of these 216 birds, 194 (90%) were held at eight museums in Canada, the US, and the UK (see Acknowledgements for all sources) with the remainder represented by feathers collected in the field. In total, of the feathers we sampled 138 were adult primaries, 55 adult head feathers, and 77 sub-adult primaries, with an average of 11 primary feathers per decade (with the exception of the years from 1860 – 1899, when only 10 museum specimens were available). To estimate diet of breeding adults, we used a section (~1 x 2 cm) cut from the tip of the innermost primary feathers as the first of these (P1) are generally moulted from mid-April to early May (Verbeek 1979), ca. 2 – 4 weeks before the lay date of first eggs (mid- to late May; Verbeek 1986; Blight

2011). Thus, isotope ratios in P1 feathers reflected a breeding bird’s diet immediately prior to and during egg production the previous year. (Innermost primaries also had the advantage of being hidden from view in standard museum specimens, so that sampling did not alter external specimen appearance.) We obtained samples from each decade from 1860 – 2009 (except the 1870s; no specimens available), targeting P1, or P2 if P1 was absent. On rare occasions when P1 and P2 were absent, we sampled P3. We also collected moulted primaries in 2008 and 2009 (P1, This article is protected by copyright. All rights reserved.

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P2, and possibly P3 given appearance and timing; Verbeek 1979) from the ground in the glaucous-winged gull colony at Mandarte Island, British Columbia (48.63°N, 123.28°W). Moulted feathers were collected from across the colony (c. 1800 breeding pairs) to minimise the chance that any individual was sampled more than once. Adult brown-tipped (hereafter, “winter”) head feathers are grown during the post-breeding moult whereas white (hereafter, “summer”) head feathers are grown late winter to early spring, preceding or coincident with territory establishment (Hayward & Verbeek 2008; LKB pers. obs.). As both winter and summer head feathers are moulted at the extreme ends of the breeding season they do not entirely represent diets from critical periods (e.g., egg production and chick rearing), but as samples they have the advantage of causing minimal alteration to museum specimens. We therefore sampled from a subset of winter and summer adult head feathers taken from the same museum specimens to ask if these could be used as a proxy indicator of long-term diet change (i.e., by showing the same trends and isotope values as primary feathers grown during breeding). As we were also interested in long-term differences in the diet of adult and sub-adult gulls, we used the above protocol to sample primary feathers from museum specimens of sub-adults. Subadult birds moult their first primaries at a similar time as adults, but sub-adult head feather moult patterns can be more variable (Howell & Dunn 2007; P. Pyle, pers comm.), and thus a poor season-specific indicator of dietary change. For this reason we did not sample sub-adult head feathers from museum specimens. Feather samples were prepared by soaking for 24 h in a 2:1 chloroform:methanol solution, and then rinsing in clean solution. Cleaned and rinsed samples were air dried in a fume hood for 48 h before loading 0.25 to 0.55 mg into tin capsules. All samples were processed at the Queen’s Facility for Isotope Research, Kingston, Ontario, using a ThermoFinnigan Delta Plus XP mass This article is protected by copyright. All rights reserved.

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spectrometer interfaced to a Costech elemental analyser for C and N isotope measurements. We ran 10% (n=27) duplication on feather samples, producing a repeatability of within